Skip to main content
SpringerLink
Log in

Mn K-edge X-ray absorption studies of mononuclear Mn(III)–hydroxo complexes

  • Original Paper
  • Published:
JBIC Journal of Biological Inorganic Chemistry Aims and scope Submit manuscript

Abstract

Mn K-edge X-ray absorption spectroscopy experiments were performed on the solid- and solution-phase samples of [MnII(dpaqR)](OTf) (R=H, Me) and [MnIII(OH)(dpaqR)](OTf). The extended X-ray absorption fine structure (EXAFS) data show distinct differences between the MnII and MnIII–OH complexes, with fits providing metric parameters in excellent agreement with values from X-ray crystallography and density functional theory (DFT) computations. Evaluation of the EXAFS data for solid-phase [MnIII(OH)(dpaq)](OTf) resolved a short Mn–OH bond distance of 1.79 Å; however, the short trans-amide nitrogen bond of the supporting ligand precluded the resolution of the Mn–OH bond distance in the corresponding solution-phase sample and for both [MnIII(OH)(dpaqMe)](OTf) samples. The edge energy also increases by approximately 2 eV from the MnII to the MnIII–OH complexes. Experimental pre-edge analysis shows the MnII complexes to have pre-edge areas comparable to the MnIII–OH complexes, despite the presence of the relatively short Mn–OH distance. Time-dependent density functional theory (TD-DFT) computations illustrate that Mn 3d–4p mixing, a primary contributor to pre-edge intensities, decreases by ~ 0.3% from the MnII to MnIII–OH complexes, which accounts for the very similar pre-edge areas. Collectively, this work shows that combined EXAFS and XANES analysis has great potential for identification of reactive MnIII–OH intermediates, such as those proposed in enzyme active sites.

Graphical Abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Scheme 1
Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Bull C, Niederhoffer EC, Yoshida T, Fee JA (1991) J Am Chem Soc 113:4069–4076

    Article  CAS  Google Scholar 

  2. Rulíšek L, Ryde U (2006) J Phys Chem B 110:11511–11518

    Article  PubMed  Google Scholar 

  3. Wennman A, Oliw EH, Karkehabadi S, Chen Y (2016) J Biol Chem 291:8130–8139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Wennman A, Karkehabadi S, Oliw EH (2014) Arch Biochem Biophys 555–556:9–15

    Article  PubMed  Google Scholar 

  5. Su C, Oliw EH (1998) J Biol Chem 273:13072

    Article  CAS  PubMed  Google Scholar 

  6. Su C, Sahlin M, Oliw EH (2000) J Biol Chem 275:18830–18835

    Article  CAS  PubMed  Google Scholar 

  7. Gaffney BJ, Su C, Oliw EH (2001) Appl Magn Reson 21:413–424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Pecoraro VL, Hsieh WY (2008) Inorg Chem 47:1765–1778

    Article  CAS  PubMed  Google Scholar 

  9. McEvoy JP, Brudvig GW (2006) Chem Rev 106:4455–4483

    Article  CAS  PubMed  Google Scholar 

  10. Glockner C, Kern J, Broser M, Zouni A, Yachandra V, Yano J (2013) J Biol Chem 288:22607–22620

    Article  PubMed  PubMed Central  Google Scholar 

  11. Yano J, Yachandra V (2014) Chem Rev 114:4175–4205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Rice DB, Wijeratne GB, Burr AD, Parham JD, Day VW, Jackson TA (2016) Inorg Chem 55:8110–8120

    Article  CAS  PubMed  Google Scholar 

  13. Wijeratne GB, Corzine B, Day VW, Jackson TA (2014) Inorg Chem 53:7622–7634

    Article  CAS  PubMed  Google Scholar 

  14. Coggins MK, Brines LM, Kovacs JA (2013) Inorg Chem 52:12383–12393

    Article  CAS  PubMed  Google Scholar 

  15. Goldsmith CR, Cole AP, Stack TDP (2005) J Am Chem Soc 127:9904–9912

    Article  CAS  PubMed  Google Scholar 

  16. Yano J, Kern J, Irrgang KD, Latimer MJ, Bergmann U, Glatzel P, Pushkar Y, Biesiadka J, Loll B, Sauer K, Messinger J, Zouni A, Yachandra VK (2005) Proc Natl Acad Sci U S A 102:12047–12052

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Frank P, Benfatto M, Qayyam M, Hedman B, Hodgson KO (2015) J Chem Phys 142:084310

    Article  PubMed  PubMed Central  Google Scholar 

  18. Kau LS, Spira-Solomon DJ, Penner-Hahn JE, Hodgson KO, Solomon EI (1987) J Am Chem Soc 109:6433–6442

    Article  CAS  Google Scholar 

  19. Westre TE, Kennepohl P, DeWitt JG, Hedman B, Hodgson KO, Solomon EI (1997) J Am Chem Soc 119:6297–6314

    Article  CAS  Google Scholar 

  20. DeBeer George S, Petrenko T, Neese F (2008) J Phys Chem A 112:12936–12943

    Article  CAS  PubMed  Google Scholar 

  21. DeBeer George S, Brant P, Solomon EI (2005) J Am Chem Soc 127:667–674

    Article  CAS  Google Scholar 

  22. Leto DF, Jackson TA (2014) Inorg Chem 53:6179–6194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. England J, Martinho M, Farquhar ER, Frisch JR, Bominaar EL, Munck E, Que L Jr (2009) Angew Chem Int Ed Engl 48:3622–3626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Jackson TA, Rohde JU, Seo MS, Sastri CV, DeHont R, Stubna A, Ohta T, Kitagawa T, Munck E, Nam W, Que L Jr (2008) J Am Chem Soc 130:12394–12407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Rohde JU, Torelli S, Shan XP, Lim MH, Klinker EJ, Kaizer J, Chen K, Nam WW, Que L (2004) J Am Chem Soc 126:16750–16761

    Article  CAS  PubMed  Google Scholar 

  26. Krewald V, Lassalle-Kaiser B, Boron TT 3rd, Pollock CJ, Kern J, Beckwith MA, Yachandra VK, Pecoraro VL, Yano J, Neese F, DeBeer S (2013) Inorg Chem 52:12904–12914

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Rees JA, Martin-Diaconescu V, Kovacs JA, DeBeer S (2015) Inorg Chem 54:6410–6422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Roemelt M, Beckwith MA, Duboc C, Collomb MN, Neese F, DeBeer S (2012) Inorg Chem 51:680–687

    Article  CAS  PubMed  Google Scholar 

  29. Ravel B, Newville M (2005) J Synchrotron Radiat 12:537–541

    Article  CAS  PubMed  Google Scholar 

  30. Rehr JJ, Mustre de Leon J, Zabinsky SI, Albers RC (1991) J Am Chem Soc 113:5135–5140

    Article  CAS  Google Scholar 

  31. Wojdyr M (2010) J Appl Crystallogr 43:1126–1128

    Article  CAS  Google Scholar 

  32. Neese F (2012) Wiley Interdisciplinary reviews: computational molecular science. J Comput Sci 2:73–78

    CAS  Google Scholar 

  33. Becke AD (1986) J Chem Phys 84:4524–4529

    Article  CAS  Google Scholar 

  34. Perdew JP (1986) Phys Rev B 33:8822–8824

    Article  CAS  Google Scholar 

  35. Schäfer A, Horn H, Ahlrichs R (1992) J Chem Phys 97:2571–2577

    Article  Google Scholar 

  36. Schäfer A, Huber C, Ahlrichs R (1994) J Chem Phys 100:5829–5835

    Article  Google Scholar 

  37. Neese F (2003) J Comput Chem 24:1740–1747

    Article  CAS  PubMed  Google Scholar 

  38. Sinnecker S, Rajendran A, Klamt A, Diedenhofen M, Neese F (2006) J Phys Chem A 110:2235–2245

    Article  CAS  PubMed  Google Scholar 

  39. Hirata S, Head-Gordon M (1999) Chem Phys Lett 302:375–382

    Article  CAS  Google Scholar 

  40. Hirata S, Head-Gordon M (1999) Chem Phys Lett 314:291–299

    Article  CAS  Google Scholar 

  41. Becke AD (1993) J Chem Phys 98:5648–5652

    Article  CAS  Google Scholar 

  42. Lee C, Yang W, Parr RG (1988) Phys Rev B 37:785–789

    Article  CAS  Google Scholar 

  43. Weigend F, Ahlrichs R (2005) Phys Chem Chem Phys 7:3297–3305

    Article  CAS  PubMed  Google Scholar 

  44. Lenthe EV, Baerends EJ, Snijders JG (1993) J Chem Phys 99:4597–4610

    Article  Google Scholar 

  45. van Wüllen C (1998) J Chem Phys 109:392–399

    Article  Google Scholar 

  46. Ciringh Y, Gordon-Wylie SW, Norman RE, Clark GR, Weintraub ST, Horwitz CP (1997) Inorg Chem 36:4968–4982

    Article  CAS  Google Scholar 

  47. Ching WM, Zhou A, Klein J, Fan R, Knizia G, Cramer CJ, Guo Y, Que L Jr (2017) Inorg Chem 56:11129–11140

    Article  CAS  PubMed  Google Scholar 

  48. Leto DF, Ingram R, Day VW, Jackson TA (2013) Chem Commun 49:5378–5380

    Article  CAS  Google Scholar 

  49. Colmer HE, Howcroft AW, Jackson TA (2016) Inorg Chem 55:2055–2069

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by NSF Grant 1565661. Use of the Stanford Synchrotron Radiation Lightsource, SLAC National Accelerator Laboratory, is supported by the US Department of Energy, Office of Science, Office of Basic Energy Sciences under Contract No. DE-AC02-76SF00515. The SSRL Structural Molecular Biology Program is supported by the DOE Office of Biological and Environmental Research, and by the National Institutes of Health, National Institute of General Medical Sciences (including P41GM103393). The contents of this publication are solely the responsibility of the authors and do not necessarily represent the official views of NIGMS or NIH. Use of Beamline 2-2 at SSRL was partially supported by the National Synchrotron Light Source II, Brookhaven National Laboratory, under US Department of Energy Contract No. DE-SC0012704. XAS experiments were supported by the Case Western Reserve University Center for Synchrotron Biosciences NIH Grant, P30-EB-009998, from the National Institute of Biomedical Imaging and Bioengineering (NIBIB). We thank Dr. Erik Farquhar at NSLS for outstanding support of our XAS experiments and for helpful conversations.

Author information

Authors and Affiliations

  1. Department of Chemistry and Center for Environmentally Beneficial Catalysis, University of Kansas, Lawrence, KS, 66045, USA

    Derek B. Rice, Gayan B. Wijeratne & Timothy A. Jackson

Authors
  1. Derek B. Rice
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gayan B. Wijeratne
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Timothy A. Jackson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Timothy A. Jackson.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 1273 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rice, D.B., Wijeratne, G.B. & Jackson, T.A. Mn K-edge X-ray absorption studies of mononuclear Mn(III)–hydroxo complexes. J Biol Inorg Chem 22, 1281–1293 (2017). https://doi.org/10.1007/s00775-017-1501-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00775-017-1501-0

Keywords

Search

Navigation